Abstract
Reports of bovine listeriosis in Brazil are uncommon, being restricted to citations within retrospective studies, resulting in scarce documented information of this important disease of cattle. This manuscript describes the molecular findings associated with spontaneous encephalitic listeriosis in two steers from distinct herds within the state of Paraná, southern Brazil. Both animals demonstrated altered consciousness suggestive of brain stem dysfunctions and died a few days after the initial onset of disease. Polymerase chain reaction (PCR) assays were designed to target specific genes of infectious neurological agents of cattle. These included bovine herpesvirus 1 and 5 (BoHV-1 and BoHV-5), ovine herpesvirus 2 (OvHV-2), Listeria monocytogenes, and Histophilus somni. Rabies virus was discarded in evaluations done at the official state diagnostic laboratory. Gross alterations were insignificant; histopathology demonstrated rhombencephalitis associated with macrophage-predominant, multifocal to coalescing microabscesses and extensive perivascular cuffings in both steers. The L. monocytogenes PCR assay amplified the 172-bp amplicon of the listeriolysin gene from the brain stem of both animals and from the telencephalon, thalamus, and cerebellum of one of them. Phylogenetic analyses demonstrated that the strains derived from this study clustered with known strains of L. monocytogenes lineage I. The BoHV-1 and BoHV-5, OvHV-2, and H. somni PCR assays were negative. These results confirm the participation of L. monocytogenes lineage I in the etiopathogenesis of the neurological disease herein described and represent the first complete description of encephalitic listeriosis in cattle from Brazil.
Similar content being viewed by others
References
Alfieri, A.A., Parazzi, M.E., Takiuchi, E., Medici, K.C., Alfieri, A.F. 2006. Frequency of group A rotavirus in diarrhoeic calves in Brazilian cattle herds, 1998–2002. Tropical Animal Health and Production, 38:521–526.
Angen, O., Ahrens, P., Tegtmeier, C. 1998. Development of a PCR test for identification of Haemophilus somnus in pure and mixed cultures. Veterinary Microbiology, 63:39–48.
Barancelli, G.V., Silva-Cruz, J.V., Porto, E., Oliveira, C.A.F. 2011. Listeria monocytogenes: occurrence in dairy products and its implications in public health. Arquivos do Instituto Biológico, 78:155.
Baxter, S.I., Pow, I., Bridgen, A., Reid, H.W. 1993. PCR detection of the sheep-associated agent of malignant catarrhal fever. Archives of Virology, 132:145–159.
Boom, R., Sol, C.J., Salimans, M.M., Jansen, C.L., Wertheim-van Dillen, P.M., van der Noordaa, J. 1990. Rapid and simple method for purification of nucleic acids. Journal of Clinical Microbiology, 28:495–503.
Brugère-Picoux, J. 2008. Ovine listeriosis. Small Ruminant Research, 76 12–20.
Claus, M.P., Alfieri, A.F., Folgueras-Flatschart, A.V., Wosiacki, S.R., Medici, K.C., Alfieri, A.A. 2005. Rapid detection and differentiation of bovine herpesvirus 1 and 5 glycoprotein C gene in clinical specimens by multiplex-PCR. Journal of Virological Methods, 128:183–188.
de Lahunta, A., Divers, T.J. 2008. Neurological diseases. In: Divers, T.J., Peek, S.F. (eds) Rebun’s Diseases of dairy cattle. 2 edn. Saunders/Elsevier, St. Louis, Missouri, p 504–560
den Bakker, H.C., Didelot, X., Fortes, E.D., Nightingale, K.K., Wiedmann, M. 2008. Lineage specific recombination rates and microevolution in Listeria monocytogenes. BMC Evolutionary Biology, 8:277.
Deneer, H.G., Boychuk, I. 1991. Species-specific detection of Listeria monocytogenes by DNA amplification. Applied and Environmental Microbiology, 57:606–609.
Galiza, G.J.N., Silva, M.L.C.R., Dantas, A.F.M., Simões, S.V.D., Riet-Correa, F. 2010. Doenças do sistema nervoso de bovinos no semiárido nordestino. Pesquisa Veterinária Brasileira, 30:267–276.
George, L.W. 2009. Listeriosis. In: Smith, B. P. (ed) Large Animal Internal Medicine. 4th edn. Mosby/Elsevier, St. Louis, Missouri, p 1045–1048
Guedes, K.M.R., Riet-Correa, F., Dantas, A.F.M., Simões, S.V.D., Miranda Neto, E.G., Nobre, V.M.T., Medeiros, R.M.T. 2007. Doenças do sistema nervoso central em caprinos e ovinos no semi-árido. Pesquisa Veterinária Brasileira, 27:29–38.
Hall, T.A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41:95–98.
Headley, S.A., Bodnar, L., Fritzen, J.T.T., Rodrigues, W.B., Bronkhorst, D.E., Alfieri, A.F., Okano, W., Alfieri, A.A. 2013a. Histopathological and molecular characterization of encephalitic listeriosis in small ruminants from northern Paraná, Brazil. Brazilian Journal of Microbiology, (Accepted)
Headley, S.A., Oliveira, V.H.S., Freire, G.F., Bronkhorst, D.E., Alfieri, A.F., Okano, W., Alfieri, A.A. 2013b. Histophilus somni-induced infections in cattle from southern Brazil. Tropical Animal Health and Production, DOI 10.1007/s11250-013-0402-7
Headley, S.A., Sousa, I.K.F., Minervino, A.H.H., Barros, I.O., Barrêto Júnior, R.A., Alfieri, A.F., Ortolani, E.L., Alfieri, A.A. 2012. Molecular confirmation of ovine herpesvirus 2-induced malignant catarrhal fever lesions in cattle from Rio Grande do Norte, Brazil. Pesquisa Veterinária Brasileira, 32:1213–1218.
Jeffers, G.T., Bruce, J.L., McDonough, P.L., Scarlett, J., Boor, K.J., Wiedmann, M. 2001. Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiology, 147:1095–1104.
Johnson, G.C., Fales, W.H., Maddox, C.W., Ramos-Vara, J.A. 1995. Evaluation of laboratory tests for confirming the diagnosis of encephalitic listeriosis in ruminants. Journal of Veterinary Diagnostic Investigation, 7:223–228.
Kumar, H., Singh, B.B., Bal, M.S., Kaur, K., Singh, R., Sidhu, P.K., Sandhu, K.S. 2007. Pathological and epidemiological investigations into listerial encephalitis in sheep. Small Ruminant Research, 71:293–297.
Liu, D. 2006. Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen. J Med Microbiol, 55:645–659.
Liu, D., Lawrence, M.L., Wiedmann, M., Gorski, L., Mandrell, R.E., Ainsworth, A.J., Austin, F.W. 2006. Listeria monocytogenes subgroups IIIA, IIIB, and IIIC delineate genetically distinct populations with varied pathogenic potential. Journal of Clinical Microbiology, 44:4229–4233.
Maxie, M.G., Youssef, S. 2007. Nervous system. In: Maxie, M. G. (ed) Jubb, Kennedy, and Palmer’s Pathology of domestic animals. vol 1, 5th edn. Saunders/Elsevier, Philadelphia, p 405–408
McGill, I.S., Wells, G.A. 1993. Neuropathological findings in cattle with clinically suspect but histologically unconfirmed bovine spongiform encephalopathy (BSE). Journal of Comparative Pathology, 108:241–260.
McLaughlin, B.G., Greer, S.C., Singh, S. 1993. Listerial abortion in a llama. Journal of Veterinary Diagnostic Investigation, 5:105–106.
Morin, D.E. 2004. Brainstem and cranial nerve abnormalities: listeriosis, otitis media/interna, and pituitary abscess syndrome. The Veterinary Clinics of North America Food Animal Practice, 20:243–273, vi.
Nightingale, K.K., Schukken, Y.H., Nightingale, C.R., Fortes, E.D., Ho, A.J., Her, Z., Grohn, Y.T., McDonough, P.L., Wiedmann, M. 2004. Ecology and transmission of Listeria monocytogenes infecting ruminants and in the farm environment. Applied and Environmental Microbiology, 70:4458–4467.
Oevermann, A., Botteron, C., Seuberlich, T., Nicolier, A., Friess, M., Doherr, M.G., Heim, D., Hilbe, M., Zimmer, K., Zurbriggen, A., Vandevelde, M. 2008. Neuropathological survey of fallen stock: active surveillance reveals high prevalence of encephalitic listeriosis in small ruminants. Veterinary Microbiology, 130:320–329.
Oevermann, A., Di Palma, S., Doherr, M.G., Abril, C., Zurbriggen, A., Vandevelde, M. 2010a. Neuropathogenesis of naturally occurring encephalitis caused by Listeria monocytogenes in ruminants. Brain Pathology, 20:378–390.
Oevermann, A., Zurbriggen, A., Vandevelde, M. 2010b. Rhombencephalitis caused by Listeria monocytogenes in humans and ruminants: a zoonosis on the rise? Interdisciplinary Perspectives on Infectious Diseases, 2010:632513.
Rasmussen, O.F., Skouboe, P., Dons, L., Rossen, L., Olsen, J.E. 1995. Listeria monocytogenes exists in at least three evolutionary lines: evidence from flagellin, invasive associated protein and listeriolysin O genes. Microbiology, 141 (Pt 9):2053–2061.
Ribeiro, L.A.O., Rodrigues, N.C., Fallavena, L.C.B., Oliveira, S.J., Brito, M.A. 2006. Listeriose em rebanho de ovinos leiteiros na região serrana do Rio Grande do Sul: relato de caso. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 58:316–319.
Rissi, D.R., Kommers, G.D., Marcolongo-Pereira, C., Schild, A.L., Barros, C.S.L. 2010. Meningoencefalite por Listeria monocytogenes em ovinos. Pesquisa Veterinária Brasileira, 30:51–56.
Rissi, D.R., Rech, R.R., Barros, R.R., Kommers, G.D., Langohr, I.M., Pierezan, F., Barros, C.S.L. 2006. Forma nervosa de listeriose em caprinos. Pesquisa Veterinária Brasileira, 26:14–20.
Roberts, A., Nightingale, K., Jeffers, G., Fortes, E., Kongo, J.M., Wiedmann, M. 2006. Genetic and phenotypic characterization of Listeria monocytogenes lineage III. Microbiology, 152:685–693.
Sanches, A.W.D., Langohr, I.M., Stigger, A.L., Barros, C.S.L. 2000. Diseases of the central nervous system in cattle of southern Brazil. Pesquisa Veterinária Brasileira, 20:113–118.
Schwab, J.P., Edelweiss, M.I.A., Graça, D.L. 2004. Immunohistochemical identification of Listeria monocytogenes in the brain tissue of ruminants. Revista Portuguesa de Ciências Veterinárias, 99:65–66.
Scott, P.R. 2004. Diagnostic techniques and clinicopathologic findings in ruminant neurologic disease. The Veterinary Clinics of North America Food Animal Practice, 20:215–230.
Stokol, T., Divers, T.J., Arrigan, J.W., McDonough, S.P. 2009. Cerebrospinal fluid findings in cattle with central nervous system disorders: a retrospective study of 102 cases (1990–2008). Veterinary Clinical Pathology, 38:103–112.
Summers, B.A., Cummings, J.F., de Lahunta, A. 1995. Veterinary Neuropathology. Mosby, Baltimore
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28:2731-2739
Ward, T.J., Ducey, T.F., Usgaard, T., Dunn, K.A., Bielawski, J.P. 2008. Multilocus genotyping assays for single nucleotide polymorphism-based subtyping of Listeria monocytogenes isolates. Applied and Environmental Microbiology, 74:7629–7642.
Wesley, I.V., Larson, D.J., Harmon, K.M., Luchansky, J.B., Schwartz, A.R. 2002. A case report of sporadic ovine listerial menigoencephalitis in Iowa with an overview of livestock and human cases. Journal of Veterinary Diagnostic Investigation, 14:314–321.
Wiedmann, M., Bruce, J.L., Keating, C., Johnson, A.E., McDonough, P.L., Batt, C.A. 1997. Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential. Infect Immun, 65:2707–2716.
Zachary, J.F. 2012. Listeriosis. In: Zachary, J. F., McGavin, M. D. (eds) Pathologic basis of veterinary disease. 5th edn. Elsevier/Mosby, St. Louis, Missouri, p 192–195
Acknowledgments
Drs Selwyn A. Headley, Alice F. Alfieri, Júlio A. N. Lisbôa, and Amauri A. Alfieri are recipients of the National Council for Scientific and Technological Development (CNPq, Brazil) fellowships. This study was partially funded by a joint CNPq/Ministry of Agriculture, Livestock, and Supply (MAPA) grant (protocol #578645/2008-4).
Conflict of interest
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Headley, S.A., Fritzen, J.T.T., Queiroz, G.R. et al. Molecular characterization of encephalitic bovine listeriosis from southern Brazil. Trop Anim Health Prod 46, 19–25 (2014). https://doi.org/10.1007/s11250-013-0441-0
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11250-013-0441-0